Anson H. Hines

BIOTIC RESISTANCE TO INVASION: NATIVE PREDATOR LIMITS ABUNDANCE AND DISTRIBUTION OF AN INTRODUCED CRAB

Introduced species frequently escape the natural enemies (predators, com- petitors, and parasites) that limit their distribution and abundance in the native range. This reduction in native predators, competitors, and parasites may result in ecological release in the introduced range. However, biological interactions also can limit the establishment and spread of nonnative populations. The extent to which such biotic resistance occurs is poorly resolved, especially for marine ecosystems. Here we test whether a native predator, the blue crab Callinectes sapidus, affects the abundance and geographic range of the in- troduced European green crab Carcinus maenasin eastern North America. Both crab species occur in shallow, soft-sediment habitats of bays and estuaries, and their ranges overlap in eastern North America. First, we tested for a negative relationship in the abundances of the two species from trap samples across a 640-km (5.788 latitude) coastal transect. Second, we estimated variation in predation pressure on tethered Carcinus maenas across latitude and as a function of Callinectes sapidus abundance. Third, we measured predation rates on Carcinus maenasby Callinectes sapidusin field and laboratory experiments. Our results support the hypothesis that the native predator Callinectes sapidusprovides biotic resistance to invasion and prevents the southward spread and establishment of Carcinus maenas. Within and across bays, Carcinus maenas were significantly less abundant at sites and depths with Callinectes sapiduscompared with areas lacking Callinectes sapidus. Moreover, no Carcinus maenaswere found in Chesapeake Bay, where Callinectes sapidus were most abundant. Predation of tethered Carcinus maenasincreased with Callinectes sapidusabun- dance. In laboratory and field experiments,Callinectes sapidus preyed readily on Carcinus maenas. Thus, we conclude the predation by Callinectes sapidus, alone or in combination with other factors, limits the abundance and geographic range of an invasive marine species.

DENSITY-DEPENDENT PREDATION, HABITAT VARIATION, AND THE PERSISTENCE OF MARINE BIVALVE PREY

The persistence of prey encountering intense predation varies by species, prey density, and habitat type; however, the collective impact of these factors has rarely been tested experimentally in natural marine systems. Using the thin-shelled clams Mya arenaria and Macoma balthica as prey, and the main epibenthic predator of whole adult clams, the blue crab Callinectes sapidus, we conducted a series of experiments in Chesapeake Bay tributaries that (1) links field abundance and distribution of bivalve prey species with habitat-specific mortality patterns; (2) represents the first comprehensive field test of species-specific, habitat-specific, and density-dependent mortality for subtidal, soft-bottom, deep-burrowing prey; and (3) thereby enables development of a conceptual model to be used as a heuristic tool linking predator–prey dynamics, habitat type, and evolutionary defense tactics for marine benthos. In 15 years of field monitoring, Mya was more common in sand than mud habitats, and Macoma was widely distributed and at higher densities than Mya in mud and sand. In field experiments, mortality of both Mya and Macoma was density dependent in those habitats where the clams are common. The blue crab population in the field exhibited a type III “guild functional response” on Mya in sand, and on Macoma in both mud and sand. Mortality was lower in sand than mud for Mya, and similar in mud and sand for Macoma, correlating with the high abundances of Mya in sand and Macoma in sand and mud. The persistence of large juvenile and adult bivalves when confronted with intense predation derived substantially from a low-density refuge from predation that varied in a species-specific manner with habitat type, demonstrating the species-specific importance of density and habitat to clam survival. We developed a conceptual model detailing the relative importance of behavior, morphology, habitat features, and the basic components of predator–prey interactions to the survival of bivalve molluscs. At one extreme are bivalve molluscs, such as oysters, that emphasize morphological refuges that increase the predators handling time. At the other extreme are bivalves, such as Mya and Macoma, that reduce predator encounter rates. The model is intended to be used as a heuristic tool to develop testable hypotheses.

Variable functional responses of a marine predator in dissimilar homogeneous microhabitats

Adult soft-shelled clams {Mya arenaria) persist at low densities in Chesapeake Bay sandy habitats despite intense predation by blue crabs {Callinectes sapidus). Clam persistence may be a consequence of variation in blue crab foraging rates as a function of clam density and sediment composition. In laboratory aquaria, we measured the functional responses (prey consumption per predator as a function of prey density) of large blue crabs to six densities of adult soft-shelled clams buried at natural depths in two sediment types (mud and sand). Functional responses in sand and mud were differentiated statistically by analyses of (1) residuals and residual sums of squares of discrete and continuous-time models, and (2) the exponent (3 of a general functional response model. Crab predation rates were significantly higher in mud than sand, and functional responses differed significantly between these two substrates. Blue crabs displayed type III (sigmoid) density-dependent functional responses in sand, and type II (decelerating rise to an upper asymptote) inversely density- dependent responses in mud. Risk of mortality for clams decreased sharply in sand at low densities similar to those observed in the field near the end of the annual period of active predation. These observations (1) suggest that variable blue crab functional responses result in microhabitat-specific mortality rates of benthic prey, and (2) indicate that functional responses can differ significantly according to the physical properties of topographically simple habitats.

Complex predator-prey interactions within an estuarine benthic community

Indirect predator—prey interactions have been suggested to be important in a variety of communities. However, we still understand little about the factors determining the relative importance of indirect and direct effects of predation or what forms indirect predator—prey interactions may take. We examined the direct effects of predation by an omnivorous grass shrimp. Palaemonetes pugio, and the indirect effects for prey species of interactions between this shrimp and other predators in an estuarine benthic community. Direct and indirect effects of predation were examined in the field using a combination of large— and small—scale enclosure/exclosure experiments. Specific interactions and mechanisms of effects were examined in laboratory predation studies, utilizing both two—species and multi—species systems. Grass shrimp predation reduced the densities of a variety of benthic fauna, but the effects varied seasonally and with prey size. Interactions between grass shrimp and other predators took two forms: reduction of an infaunal predator by shrimp predation and predation on grass shrimp by fish. Both types of interactions had a mixed effect on lower trophic levels, with enhancement of certain benthic prey and no effect on other species. Interactions between grass shrimp and their fish predators resulted in changes in shrimp distribution independent of changes in shrimp abundance, creating spatial refungia for shrimp prey. The dynamics of indirect interactions in this community are strongly affected by the omnivorous nature of the major predators. Our results emphasize the general importance of omnivory in regulating predator—prey interactions and in predicting the relative importance of indirect predator effects.

Spatial structure of bivalves in a sandflat:: Scale and generating processes

A survey was conducted during the summer of 1994 within a fairly homogeneous 12.5 ha area of sandflat off Wiroa Island, in Manukau Harbour, New Zealand, to identify factors controlling the spatial distributions of the two dominant bivalves, Macomona liliana Iredale and Austrovenus stutchburyi (Gray), and to look for evidence of adult–juvenile interactions within and between species. Most of the large–scale spatial structure detected in the bivalve count variables (two species, several size classes of each) was explained by the physical and biological variables. The results of principal component analysis and spatial regression modelling suggest that different factors are controlling the spatial distributions of adults and juveniles. Larger size classes of both species displayed significant spatial structure, with physical variables explaining some but not all of this variation. Smaller organisms were less strongly spatially structured, with virtually all of the structure explained by physical variables. The physical variables important in the regression models differed among size classes of a species and between species. Extreme size classes (largest and smallest) were best explained by the models; physical variables explained from 10% to about 70% of the variation across the study site. Significant residual spatial variability was detected in the larger bivalves at the scale of the study site. The unexplained variability (20 to 90%) found in the models is likely to correspond to phenomena operating at smaller scales. Finally, we found no support for adult–juvenile interactions at the scale of our study site, given our sampling scale, after controlling for the effects of the available physical variables. This is in contrast to significant adult–juvenile interactions found in smaller–scale surveys and in field experiments. Our perception of adult–juvenile interactions thus depends on the scale of study.

Invasion pressure to a ballast-flooded estuary and an assessment of inoculant survival

The relationships between invasion pressure, post-transport inoculant survival, and regional susceptibility to invasion are poorly understood. In marine ecosystems, the movement and release of ballast water from ocean-going ships provides a model system by which to examine the interplay among these factors. One of the largest estuaries in North America, the Chesapeake Bay, receives tremendous amounts of foreign ballast water annually and thus should be at high invasion risk. To date, however, few introductions in Chesapeake Bay have been attributed to ballast release. To understand better the dynamics of this invasion process, we (1) characterized and quantified the biota arriving to Chesapeake Bay in foreign ballast water, (2) compared temperatures and salinities of ballast water and harbor water in upper Chesapeake Bay, and (3) tested experimentally survival of organisms collected from ballast water in temperatures and salinities characteristic of the region. From 1993 to 1994, we sampled planktonic and benthic organisms from 60 foreign vessels arriving to Chesapeake Bay. Our data show that the estuary is being inoculated by a diverse assemblage of aquatic organisms from around the world. Furthermore, the short transit time (≤15 d) for most vessels ensured that substantial numbers of larval and post-larval organisms were being deballasted alive. Most of the ballast water discharged into the upper Chesapeake Bay, however, was significantly higher in salinity (>20‰) than that of the receiving harbor. In laboratory tolerance experiments, ballast water organisms perished under such conditions. Thus, a mismatch in physical conditions between donor and receiver regions may explain the dearth of invasions in the upper Bay. It is likely that the lower Chesapeake Bay, which is more saline, remains at higher risk to ballast water invasion. Recognition of such intraregional differences should allow more focused predictions for monitoring and management.

Scaling-up from experiments to complex ecological systems: Where to next?

a , b c d e * S.F. Thrush , D.C. Schneider , P. Legendre , R.B. Whitlatch , P.K. Dayton , a f a g h J.E. Hewitt , A.H. Hines , V.J. Cummings , S.M. Lawrie , J. Grant , a a i R.D. Pridmore , S.J. Turner , B.H. McArdle National Institute of Water and Atmospheric Research, P.O. Box 11-115, Hamilton, New Zealand Ocean Sciences Centre, Memorial University of Newfoundland, St. John’s, Canada ALC5S7 c ́ ́ ́ Departement de Sciences Biologiques, Universite de Montreal, C.P. 6128, succursale Centre-ville, ́ ́ Montreal, Quebec H3C 3J7, Canada Dept. Marine Sciences, University of Connecticut, Groton, CT 06340-6097, USA Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA 92093-0201, USA Smithsonian Environmental Research Center, P.O. Box 28, Edgewater, MD 21037, USA Culterty Field Station, University of Aberdeen, Newburgh, AB40AA, Scotland Dept. of Oceanography, Dalhousie University, Halifax, Canada B3H 4JI Biostatistics Unit, School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland, New Zealand

Nonlinear foraging response of a large marine predator to benthic prey: eagle ray pits and bivalves in a New Zealand sandflat

The density-dependent foraging response of eagle rays (Myliobatis tenuicaudatus) to infaunal bivalves (Macomona lilliana) was measured in a New Zealand sandflat. Disturbance pits provided unequivocal indicators of ray feeding activity, and pits were counted on a plot (250 m×500 m) which had prey density mapped in a 200 cell (25 m×25 m) grid. Although foraging response increased significantly with prey density treated as a nominal (class, ANOVA-type) variable, treating bivalve density as a ratio scale (continuous, regression-type) variable provided more information about characteristics of the response. Eagle rays exhibited a nonlinear segmented response to prey density, in which ray foraging activity was low and independent of prey density at low Macomona densities, while foraging increased sharply above a threshold density of prey but did not reach satiation at the highest prey densities in our site. By counting ray pits repeatedly over a 31 day period, we showed that the levels and slope of the foraging response (no. of ray pits per 707 m2 per 4 days) varied temporally during the season, but the nonlinear characteristic and the threshold of prey density were consistent. Correlation analysis showed that the distribution of bivalve prey and ray foraging was spatially constant during the season. Comparison of 3 estimators of prey density showed that a fitted polynomial density was the best predictor of ray foraging, and indicated that rays were responding to prey patches on a scale of 75–100 m. The temporal features of the response to prey density were incorporated into a nonlinear segmented model and integrated with respect to time for each cell of the study grid. The impact of ray foraging estimated from the integral indicated that only about 1.6% of the Macomona population was consumed and 5.0% of the total plot was disturbed by rays during one month of study. However, the nonlinearity of response indicated that foraging impacts were concentrated disproportionately on high density patches of prey, which suffered up to 4% mortality and 13% disturbance. Macomona gained a refuge from predation and disturbance at low density, which would stabilize prey populations and even out prey distribution.

Diel variation in predator abundance, predation risk and prey distribution in shallow-water estuarine habitats

Abstract Predation by visual predators is often affected by light conditions and may therefore exhibit strong diel variation. The dominant predators on grass shrimp, Palaemonetes pugio , are finfish predators that are thought to locate their prey by visual cues. We examined the response of grass shrimp to diel variation in predation risk in the nearshore shallow waters of the Chesapeake Bay. We used diel shoreline seines to assess the relative abundance of predators. We assessed the relative risk of predation with shrimp tethered at refuge (30 cm) and nonrefuge (60 cm) depths. To measure grass shrimp response to predation risk, we used dipnets to monitor habitat use. Four predominantly visual predators dominated the shoreline seine catches, Fundulus heteroclitus , Micropogonias undulatus , Morone americana and Morone saxatilis . Total predator abundance had a diel component, with dramatic nighttime decreases in total abundance, whereas guild composition and relative abundance remained unchanged. Relative predation risk for tethered shrimp exhibited significant time by habitat interaction. During the day, depth negatively affected survivorship of tethered shrimp while at night overall survivorship increased and there was no effect of depth. Shrimp habitats use reflected diel predation risks. Abundances in the near shore were highest during the day with decreased abundances at night. Together, the seine and tethering data highlight the importance for a refuge (e.g., shallow water) from predation during the daytime and a relaxation of predation pressure at night.

Vertical distribution of infauna in sediments of a subestuary of central Chesapeake Bay

The vertical distribution of infauna was quantified in eight strata from 0–35 cm in sand and mud sediments of a lower mesohaline subestuary of Chesapeake Bay. Large numbers of small polychaetes, amphipods, and clams occurred in the upper 5 cm of both sediment types, whereas large clams (Macoma balthica in mud andMya arenaria in sand) extended down to 30 cm and comprised most of the biomass in their respective sediment types. There was extensive overlap of the species inhabiting both sediment types. Vertical stratification within and among species apparently reflected constraints on burrowing depth related to body size rather than resource partitioning among competitors. The maximal sediment penetration of 35 cm, which was exhibited byHeteromastus filiformis, was considerably less than the maximal penetration for deep burrowing species in some marine infaunal communities. Several species which burrowed deeper than 5 cm exhibited significant temporal shifts in their vertical distribution.